Aquaculture 219 (2003) 317 – 336
www.elsevier.com/locate/aqua-online
Review
Nutrients, phytoplankton and harmful algal blooms
in shrimp ponds: a review with special reference
to the situation in the Gulf of California
R. Alonso-Rodrı́guez a,b, F. Páez-Osuna a,c,*
a
Graduate Program on Marine Sciences and Limnology, Institute of Marine Sciences and Limnology,
National Autonomous University of Mexico, P.O. Box 811, Mazatlán 82000, Sinaloa, Mexico
b
Graduate Program on Use, Management and Preservation of Natural Resources,
Center for Biological Research of the Northwest, P.O. Box 128, La Paz 23097, B.C.S., Mexico
c
Mazatlan Academic Unit of the Institute of Marine Sciences and Limnology,
National Autonomous University of Mexico, P.O. Box 811, Mazatlán 82000, Sinaloa, Mexico
Received 21 August 2001; received in revised form 16 July 2002; accepted 23 August 2002
Abstract
The present work is a first attempt to document the latest reports on the occurrence of algal
blooms in shrimp farm ponds worldwide. Particular emphasis is placed on discussing the relation of
algal blooms with nutrients, with special reference to the northwest of Mexico. Typically, shrimp
pond waters are enriched with organic matter and nutrients whose concentrations depend mostly on
the management (i.e. higher stocking densities, water use, food and fertilizers). Generally, more
intensive culture systems produce higher loads of nutrients in their discharge (e.g. N and P). Nitrogen
and P concentrations vary in pond waters; N/P ratio ranges from 1.1 to 67 with values being more
frequently between 1.1 and 6.8. Such variations are closely related with the cycling and supply of
nutrients in the ponds. In shrimp farms located in NW Mexico, phytoplankton abundance varies
widely, having a higher abundance in advanced stages of the culture cycle. In the most common
pond types (intensive and semi-intensive), Synechocystis diplococcus (cyanobacteria) was the
dominant species (>88.9%), followed by Peridinium trochoideum (Scrippsiella trochoidea) and
eventually Prorocentrum minimum and Gymnodinium spp. (dinoflagellates). The numerous
occurrences of large blooms of dinoflagellates and other functional groups such as cyanobacteria,
diatoms, chlorophytes and flagellates mean economic losses for farm industry on account of shrimp
mortality or growth diminution due to poisoning, anoxic or mucus production effects, in which
* Corresponding author. Graduate Program on Marine Sciences and Limnology, Institute of Marine Sciences
and Limnology, National Autonomous University of Mexico, P.O. Box 811, Mazatlán 82000, Sinaloa, Mexico.
Tel.: +52-669-9-852845; fax: +52-669-9-826133.
E-mail address: paezos@servidor.unam.mx (F. Páez-Osuna).
0044-8486/03/$ - see front matter D 2003 Elsevier Science B.V. All rights reserved.
PII: S 0 0 4 4 - 8 4 8 6 ( 0 2 ) 0 0 5 0 9 - 4
318
R. Alonso-Rodrı́guez, F. Páez-Osuna / Aquaculture 219 (2003) 317–336
shrimp were mortality provoked in different regions: in China, the dinoflagellates Alexandrium
tamarense (Gonyaulax tamarensis) and Gymnodinium; in Malaysia, the raphidophyte Hornellia
(Chattonella) and the dinoflagellate Pyrodinium bahamense var. compressum; in Vietnam, the
diatom Nitzchia navis-varingica; in Ecuador, the dinoflagellate Gyrodinium instriatum; and in NW
Mexico the cyanobacteria S. diplococcus, Schizothrix calcicola, and the dinoflagellates P. minimum,
and lastly Gymnodinium catenatum from supply waters.
D 2003 Elsevier Science B.V. All rights reserved.
Keywords: Shrimp culture ponds; Nutrients; Phytoplankton; Harmful algal blooms
1. Introduction
In tropical and subtropical coastal areas worldwide, no economical activity has evolved
as quickly as shrimp farming in the last 15 years. However, such an enormous development has been accompanied by strong controversies on the environmental, economic and
social impacts of shrimp farming. Mexico, as well as several nations from Asia and Latin
America, has experienced an increased expansion that concerns governmental and nongovernmental organizations (Páez-Osuna, 2001a).
Shrimp farming can produce diverse environmental impacts depending on several
factors: (a) location of farms; (b) management and use of technology during pond
operation; (c) culture surface and scale of production; and (d) depurative capacity of
receiving water body. Some effects that can be pointed out are impairment of water quality
in receiving water bodies that can result in oxygen depletion, light penetration is
diminished because of suspended solids, a hypernutrification that turns into changes of
benthic macrofauna and eutrophication of water bodies (Páez-Osuna, 2001b). This paper is
a review on the occurrence of nutrients and their relation with the abundance and
composition of phytoplankton communities, primary production and algal blooms in
shrimp farm pond waters. Additional information is provided in relation with the presence
of nutrients in adjacent water bodies that supply and receive water to and from shrimp
ponds. Also, phytoplankton species that produce toxic effects are considered. Finally,
levels and stoichiometry of nutrients in pond waters as causative agents of change in the
structure of phytoplankton communities are discussed.
2. Study area
The northwest Mexico is situated in the subtropical Pacific subzone, which extends
from Baja California southward to about 16j north latitude (Brusca and Wallerstein, 1979;
Fig. 1). The presence of many rivers with small drainage basins and a coast climate semiarid to sub-humid, becoming humid to southeast, are characteristic of this zone (Lankford,
1977). An important feature of the NW coast of Mexico is the presence of numerous
coastal lagoons, e.g. from the Colorado River in Sonora to San Blas in the state of Nayarit,
there are about 35 lagoon systems. The Mexican NW coast is characterized by the
presence of a vast agriculture (ca. 1,833,000 ha), a moderate population (ca. 6,500,000
R. Alonso-Rodrı́guez, F. Páez-Osuna / Aquaculture 219 (2003) 317–336
319
Fig. 1. Study area subject to review. Squares mean shrimp farms discussed; main sources of data for this work.
inhabitants) and, recently, the incorporation of shrimp aquaculture (ca. 26,000 ha in
operation) (Páez-Osuna et al., 1999). The most important harbors and coastal towns in
Mexico have been developed on or near to the coastal lagoon systems.
3. Nutrients and stoichiometric ratio in shrimp pond waters
Generally, waters and effluents from shrimp ponds are enriched with suspended solids,
organic matter and nutrients (Table 1); concentrations depend mainly on the management
(Páez-Osuna, 2001b). In extensive farms, wastes from ponds are scarce, while at semiintensive farms intermediate loads are discharged. It is clear that depending on the degree
of intensity (i.e. stocking density, water use, food and fertilizers), a higher waste load is
produced, as well as nitrogen and phosphorus. In effluents and pond waters, several
chemical aspects have been evaluated in different types of cultures in Asia (Phillips, 1994;
Briggs and Funge-Smith, 1994; Robertson and Phillips, 1995; Tookwinas and Songsangjinda, 1999) and the Americas (Hopkins et al., 1993; Páez-Osuna et al., 1997; Rivera-
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Table 1
Water quality of effluents from shrimp ponds and domestic waste water (mg l
1
)
Variable
Semi-intensive
Intensive
Domestic
waste watera
BOD
Total N
Total P
N/P
0.2 – 7.4
0.1 – 8.6
0.06 – 0.31
1.1 – 61
0.4 – 33.9
0.5 – 20.9
0.2 – 0.69
5.5 – 67
300
75
20
8.3
Ranges were determined from data of Páez-Osuna et al. (1994); Tunvilai et al. (1993); Robertson and Phillips
(1995); Briggs and Funge-Smith (1994); Hopkins et al. (1993).
a
Clark (1989).
Monroy et al., 1999). Nutrient levels (N and P) show such wide variations in effluents
from intensive and semi-intensive systems that it is not possible to establish differences
between both systems on the basis of nutrient concentrations through point measurements.
Intermediate and low nutrient levels are comparable to those found in pristine mangrove
waterways, so it is difficult to monitor discharges when receiving waters are eutrophic or
hypertrophic.
From literature data (Table 1) on pond water composition, variation of nitrogen and
phosphorous results in N/P ratios that range from 1.1 to 61 in semi-intensive systems and
from 5.5 to 67 in the intensive systems. However, ratios are more frequently in the range
of 1.1 to 6.8. In effluents from an intensive shrimp farm with Penaeus japonicus from the
east coast of Australia, Jones et al. (2001) reported a N/P ratio of 24 for the dissolved
fraction; however, in pond waters for the culture of Penaeus monodon in the east of
Thailand, the N/P ratio in the dissolved fraction was 1.1 (Tookwinas and Songsangjinda,
1999). Such wide variation is related to the recycling and metabolism of nutrients, as well
as with the varying nutrient composition and water supply into the ponds. In studies with
mass balances, it was concluded that N and P are supplied mainly by food and water
(Briggs and Funge-Smith, 1994; Páez-Osuna et al., 1997). The levels of N and P in water
supply depend on the degree of contamination of the water source by anthropogenic
discharges (municipal, agricultural and industrial).
Páez-Osuna et al. (1994) registered wide variations of nutrient levels from continuous
monitoring studies in the water supply of shrimp ponds in the NW of Mexico. Average
concentrations (mg l 1) were as follows: for the dry season, 0.346 of N and 0.161 of P;
and in the rainy season, 0.378 of N and 0.124 of P. The above values resulted in N/P ratios
from 12.0 to 20.6 in cases where anthropogenic activity was not evident, while in the
eutrophic waters of Mazatlán harbor, where untreated sewage from urban and seafood
activity is discharged, N/P average ratios were 8.06 in the dry season and 8.29 in the rainy
season (Alonso-Rodrı́guez et al., 2000).
Páez-Osuna et al. (1997) calculated that from the total N and P supply to the semiintensive shrimp ponds, 76% of N and 83.4% of P enters through the food. Considering
that for the NW of Mexico, food composition is 35% raw protein and 1.2% P (Páez-Osuna
et al., 1999), one would expect a similar condition in shrimp ponds with a N/P ratio of
10.3. However, since food is partly metabolized by shrimp and bacteria, and another
fraction is not consumed, there is a loss of nutrients that actually goes to the pond and
R. Alonso-Rodrı́guez, F. Páez-Osuna / Aquaculture 219 (2003) 317–336
321
alters the composition of the pond water. For a semi-intensive system with a production of
1.8 tons ha 1, an apparent loss of 54.4 kg of N and 21.4 of P was calculated (Páez-Osuna
et al., 1997), i. e. a N/P ratio of 6.6; and a mean stoichiometric N/P ratio of 6.8 F 9.1 for
the dry season.
Pond management is essential for a productive shrimp farm. In this sense, adequate
nutrient levels will allow the right biomass and structure of phytoplankton. An excessive
supply of nutrients, as is the case in coastal waters, will result in an over-enrichment that
eventually will promote algal blooms, primary productivity and growth of some macrophytes. Additionally, nutrients in excess will alter phytoplankton composition with a
resulting change of dominant species; such changes imply the substitution of larger species
for smaller ones and the replacement of diatoms by dinoflagellates. In NW Mexico, a
similar, but less frequent, condition has been observed in shrimp farm ponds where
filamentous macroalgae (Enteromorpha intestinalis) occur, inhabitant species of highly
eutrophic estuaries (Kamer et al., 2001).
Algal blooms can produce hypoxia or anoxia with resulting shrimp mortality. In NW
Mexico, it is a sporadic event that takes place at dawn when a set of conditions coincides:
cloudy days, calm winds and neap tides. These events are highly expensive for shrimp
farming. Anoxic episodes can change community structure inside and outside the shrimp
ponds because sessile and non-sessile communities are affected. As a result of the changes
in biota, nutrient release from sediments is enhanced.
4. Coastal waters as sources of phytoplankton for shrimp ponds
In most shrimp farms from the Gulf of California, coastal waters are used for supplying
shrimp ponds; in some cases water is pumped directly from the coast and in other cases
indirectly through coastal lagoons. In the Gulf of California, the most abundant and
diverse groups of the phytoplankton are diatoms (415 species) and dinoflagellates (270
species) (Licea et al., 1995; Moreno et al., 1996).
Frequently, biomass of small producers is higher than biomass represented by bigger
species. In the tropical Pacific, for instance, picoplankton ( < 2 Am) accounts for 39 –63%
of total chlorophyll (being the group of cyanobacteria the most abundant); nannoplankton
(from 2 to 20 Am) represents 27 –42% and microplankton (>20 Am) accounts for 9 –16%
(Peña et al., 1990). Diverse studies in the Gulf of California have shown the significant
contribution of nannoplankton to primary production (Table 2).
Santoyo (1994) reported that diatoms constitute around 90% of the aquatic community
of coastal lagoons in Mexico; however, a review of the literature indicates that diatoms
Table 2
Contribution of nannoplankton to primary productivity from different regions in the Gulf of California
Location
Season
Nannoplankton (%)
Reference
Central gulf
15 coastal lagoons
Gulf of California
Central gulf
spring
summer
autumn
winter
>70
50 – 75
72
65 – 97
Lara-Lara and Valdéz-Holguı́n (1988)
Gilmartin and Revelante (1978)
Zeitzschel (1970)
Gaxiola-Castro et al. (1995)
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R. Alonso-Rodrı́guez, F. Páez-Osuna / Aquaculture 219 (2003) 317–336
comprise about 70% both as species number or relative abundance (Table 3). Depending
on several factors in coastal lagoons, there are dominant groups: diatoms, dinoflagellates,
cyanobacteria, chlorophytes, phytoflagellates, silicoflagellates and euglenophytes. Among
the most important variables for the dominance of a given group, there are sources of water
supply (a river or the sea), salinity and dynamic aspects of a lagoonal system (e.g. tidal
regime, stratification, water exchange).
In coastal lagoons, neritic and oceanic species can be very abundant. Phytoplankton
abundance in the coastal lagoons of NW Mexico ranges from 1 103 to 13 106 cells
l 1. An elevated concentration of 72 106 cells l 1 was reported for Estero de Urı́as,
Sinaloa (Pastén-Miranda, 1983; Santoyo, 1994).
Most frequent and abundant diatoms in coastal lagoons of Mexico come from the
marine environment, and they are mostly neritic. In contrast, in the inner parts of lagoons,
diatoms are frequently benthic (Santoyo, 1994). The most microalgae are obligate
photoautotrophs, and their growth is strictly dependent of photosynthetic activity; in the
case of dinoflagellates, the nutritional strategies are diversed, and show varying degrees of
mixotrophy and heterotrophy through a combination of phototrophy and phagotrophy in
response to rapid changes in the environmental conditions such as light availability,
inorganic and organic nutrient concentrations and food particle abundance (Bouvier et al.,
1998; Stickney et al., 2000).
Cyanobacteria, a group that survive under extreme conditions, are highly dominant
during the winter in shallow waters with low or null currents and high nutrient supply
(Santoyo, 1972). Among chlorophytes, several genus have been registered during the
winter, when fresh water supply occurs (Gómez-Aguirre et al., 1974a; Table 4). Silicoflagellates and coccolitophorids are poorly represented in coastal lagoons from the NW
Mexico (Gómez-Aguirre and Santoyo, 1975; Table 4).
Species succession in aquatic environments starts with small flagellates and diatoms,
then dinoflagellates of big size. In coastal lagoons, there is a final step that includes
Table 3
Annual relative abundance of diatoms in coastal water bodies from NW Mexico
Water body
Diatom
abundance (%)
Reference
Magdalena – Almejas Lagoon
60a
La Paz Bay
San Lorenzo Channel
Central Gulf of California
Yavaros Lagoon
Mazatlán Bay
Mazatlán Bay and Estero de Urı́as, Lagoon
Estero del Pozo Lagoon; Teacapán and
Chametla inlets
55a
85b
60a
80b
70b
70a
56a
Gárate-Lizárraga and Verdugo-Dı́az
(2000)
Signoret and Santoyo (1980)
Lavaniegos and López-Cortés (1997)
Gárate-Lizárraga et al. (1990)
Santoyo (1972)
Alonso-Rodrı́guez (1998)
Priego-Martı́nez (1985)
Gómez-Aguirre and Santoyo (1975)
a
b
Obtained with respect to total number of taxa.
Obtained with respect to total volume of sample.
R. Alonso-Rodrı́guez, F. Páez-Osuna / Aquaculture 219 (2003) 317–336
323
Table 4
Representative phytoplankton genera in coastal lagoons from NW Mexico
Planktonic diatoms
Benthic diatoms
Dinoflagellates
Cyanobacterias
Chlorophytes
Silicoflagellate
Bacteriastrum
Cerataulina
Chaetoceros
Coscinodiscus
Hemiaulus
Lauderia
Leptocylindrus
Pseudonitzchia
Skeletonema
Rhizosolenia
Thalassiosira
Amphiprora
Amphora
Coconeis
Gyrosigma
Melosira
Navicula
Pleurosigma
Synedra
Thalassionema
Thalassiotrix
Ceratium
Dinophysis
Gonyaulax
Gymnodinium
Gyrodinium
Noctiluca
Prorocentrum
Protoperidinium
Pyrophacus
Pyrocystis
Scrippsiella
Anabaena
Anabaenopsis
Chroococcus
Gloeocapsa
Merismopedia
Microcystis
Nostoc
Oscillatoria
Ankistrodesmus
Chlamydomonas
Cosmarium
Oedogonium
Pediastrum
Scenedesmus
Volvox
Dictyocha
Source: Gómez-Aguirre (1972); Gómez-Aguirre and Martı́nez-Córdova (1998); Gómez-Aguirre and Santoyo
(1975); Gómez-Aguirre et al. (1974a,b); Santoyo (1972, 1994); Licea et al. (1999); Bustillos-Guzmán (1986);
Gilmartin and Revelante (1978).
cyanobacteria, a group that thrives under stressing conditions for other organisms and
when nitrogen compounds are scarce (Margalef, 1969).
Estuaries and coastal lagoons are areas of high productivity; they also work as
reproductive sites for important aquatic resources (Cárdenas, 1969). From diverse studies
in the NW Mexico region, it can be said that phytoplankton is the most important
Table 5
Net primary productivity and dominant communities in coastal water bodies from NW Mexico
Water body
Productivity
(g C m 2 year
1
)
Dominant
community
Reference
Bustillos-Guzmán and
Olivares-González (1986)
Valdéz-Holguı́n and
Martı́nez-Córdova (1993)
Paredes-Romero and
López-Torres (1988)
Cid-Becerra and
Lares-Leyva (1988)
Flores-Verdugo et al. (1988)
Balandra Lagoon
74a
De La Cruz Lagoon
188a
Tastiota Lagoon
145a
La Lechuguilla Lagoon
208a
El Verde Lagoon
470a
Estero de Urı́as Lagoon
Teacapán – Agua Brava Lagoon
Huizache – Caimanero Lagoon
Pacific Ocean
(tropical and subtropical zones)
Semi-intensive shrimp ponds
(southern Sinaloa)
Extensive shrimp ponds (Vietnam)
620a
150a
453a
427a
phytoplankton,
macrophytes
phytoplankton,
macrophytes
phytoplankton,
macrophytes
phytoplankton,
macrophytes
phytoplankton,
macrophytes
phytoplankton
phytoplankton
phytoplankton
phytoplankton
562 F 224b
phytoplankton
Guerrero-Galván (1994)
0 – 412a
phytoplankton,
bacterioplankton
Alongi et al. (1999)
a
b
Robles-Jarero (1985)
Flores-Verdugo et al. (1990)
Arenas (1979)
Vinogradov et al. (1997)
Values obtained by the O2 liberation method (Strickland and Parsons, 1972).
Values obtained by diurnal curve method (Reyes and Merino, 1991) during the dry cycle from four ponds.
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R. Alonso-Rodrı́guez, F. Páez-Osuna / Aquaculture 219 (2003) 317–336
contributor to primary production. These water bodies, whether they have an ephemeral or
permanent mouth, export organic matter during the rainy season (in the summer) and
import it during the dry season (in the winter) from coastal upwelling supply. However,
after a balance of both events, there is a net exportation of organic matter (Flores-Verdugo
et al., 1995).
Annual primary production shows seasonal variations, with phytoplankton blooms in
the rainy season due to the occurrence of nutrients from runoff. Turbidity associated with
heavy rains block light penetration resulting in a phytoplankton biomass decrease. After
the above turbidity event and when settlement of particle ends, a second blooms starts by
the beginning of winter (Flores-Verdugo et al., 1995).
The high productivity in these water bodies nourishes fisheries that are important on a
regional and national basis. If a range of 301 to 500 g C m 2 year 1 in a lagoon is
considered as eutrophic (Pitta et al., 1999), then half of the lagoons considered in this
study are eutrophic. From the scarce information on this matter, it can be stated that
primary production in shrimp farm ponds is comparable to that of the most productive
coastal lagoons and estuaries of NW Mexico (Table 5).
5. Phytoplankton in shrimp ponds
Microalgae from water bodies that supply water are founding the early stages in shrimp
farm ponds. Phytoplankton composition and abundance in supply water is modified in
shrimp ponds. In some culturing systems, where salinity decreases because of the mixing
with fresh water from rivers, there are ponds where diatoms, cyanobacteria, chlorophytes
and dinoflagellates dominate, depending on several environmental factors (e.g. light,
salinity, temperature and nutrient levels). The occurrence of some species can be temporal
or can last longer. Sometimes there are blooms of short periods, but a very high abundance
of one or a few species that can alter shrimp growth due to oxygen depletion at nights
(depending on density, dominant species and bloom duration).
Within the first weeks of the culture (when shrimp change from postlarvae to juvenile),
specimens feed on microalgae and planktonic copepods, detritus and mollusk larvae. In
semi-intensive systems, food supply starts 2 months after the stocking, depending on the
quality of supplied water since postlarvae feed on the naturally occurring food (Fast,
1992).
The main contribution of phytoplankton to the sub-adult and adult stages of cultured
shrimp is through the trophic chain: shrimp can feed on macrofauna such as small bivalves
and gasteropods; on meiofauna such as polychaetes, amphipods and harpacticoid copepods; and on meiobenthos such as bacteria and detritus. Shrimp also consumes phytoplankton when it is adhered to detritus (Gómez-Aguirre and Martı́nez-Córdova, 1998).
Protein, lipid and carbohydrate content in phytoplankton vary among species and
because of environmental factors. With respect to amino acid content, almost all microalgae have a similar composition (Brown et al., 1997). Microalgae can also produce side
products that are toxic for diverse organisms including man (Anderson et al., 2001).
According to Boyd (1989), diatoms enhance growth better than cyanobacteria. Most
shrimp farm managers prefer a high ratio of diatoms in a phytoplankton community; this is
R. Alonso-Rodrı́guez, F. Páez-Osuna / Aquaculture 219 (2003) 317–336
325
accomplished by repeated small amounts of fertilizers that results in a N/P ratio of 20:1
(Boyd and Daniels, 1993).
Shrimp diseases not specified in Chinese farms were preceded by the following
conditions: decrease of chlorophyll a, increase of pheophytin, 68– 74% nannoplankton,
20 –27% picoplankton, 4.2 –5% microplankton, normal levels of nitrogen and a steep
increase of phosphate (Hiu et al., 1998).
Boyd (1989) has established that diatoms are the dominant phytoplankton group in
ponds with brackish waters, while cyanobacteria dominate in ponds with waters of lower
salinities in temperate waters. Nevertheless, in shrimp farms from NW Mexico, cyanobacteria was the dominant group, followed by dinoflagellates and diatoms (CortésAltamirano et al., 1994); a similar situation has been reported in other subtropical regions
of the world (Rungsupa et al., 1999). Diel variations of phytoplankton in a semi-intensive
farm from NW Mexico showed that to salinities 16 – 20, dominant species were
cyanobacteria (Synechocystis diplococcus and Oscillatoria limnetica) and a dinoflagellate
(Prorocentrum minimum) (Cortés-Altamirano et al., 1995).
In another study (March –July, 1993), in two shrimp farms located in southern Sinaloa,
N/P ratios were 6.8 for a semi-intensive system and 3.6 for an intensive system (BarrazaGuzmán, 1994). In both farms, cyanobacteria were dominant, with a highest abundance of
3.5 106 cells l 1; other important groups were diatoms, dinoflagellates and phytoflagellates. Euglenophytes were also registered during the culture cycle.
In a comparative study in four shrimp farms from NW Mexico (Fig. 1) (CortésAltamirano et al., 1994), the highest diversity (39 and 42 species) was registered for
two intensive ponds (20 – 50 pl m 2). In the case of the two semi-intensive ponds (8 –
20 pl m 2), species diversity was lower (31 and 34 species). In the spring– summer
term, diatoms were the group with the highest diversity but lowest abundance for the
pond and supply waters. Cyanobacteria were the second most diverse group with 6
(intensive system) and 12 (semi-intensive system) species, mostly nannoplanktonic
species. Cyanobacteria were highly abundant in all shrimp farms. Dinoflagellate was
the least abundant group. In a general way, the four shrimp farms showed a wide
variation of phytoplankton abundance in quantitative terms; density was always higher
in shrimp ponds than in reservoirs, but it increased according to the culture cycle, with
a final decrease at the end of the crop. Such variations result by diverse factors: supply
of food and fertilizers, changes in the rates of exchange waters and zooplankton
grazing. During the study, some rain may have influenced phytoplankton populations.
In semi-intensive pond waters, when phytoplankton barely exceeded 1 106 cells l 1,
it was mainly composed of nannoplankton (2 –20 Am length) communities. It has been
observed that after the first half of the culture cycle, density in intensive and semiintensive systems was higher than 1 106 cells l 1. Another peculiar aspect of the
studied shrimp farms is that those ponds that have been in operation for more than 3
years had higher densities than ponds that were recently incorporated (Cortés-Altamirano et al., 1994).
For all the studied ponds in the four shrimp farms from NW Mexico, cyanobacteria was
the dominant group numerically, and with the exception of an intensive farm (89%),
abundance was always >98%. The above results agree with the observations of Sevrin and
Pletikosic (1990) for a higher abundance of cyanobacteria during summer.
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Table 6
Summary of the more abundant microalgae species (>1 106 cellsl
Mexico
1
) occurring in shrimp ponds from NW
Bacillariophyceae
Dinophyceae
Cyanophyceae
Achnantes sp.
Cyclotella kuetzingiana
Cyclotella spp.
Navicula spp.
Nitzschia closterium
Nitzschia radiosa.
Nitzschia spp.
Amphidinium sp.
Gymnodinium incoloratum
Gyrodinium sp.
Gyrodinium spirale
Prorocentrum minimum
Scrippsiella trochoidea
Anabaena aequalis
Anabaenopsis elenkinii
Anabaenopsis arnoldi
Micrococcus spp.
Oscillatoria limnetica
Protococcus spp.
Schizothrix calcicola
Synechocystis diplococcus
Synechocystis leopoliensis
Spirulina spp.
Data from Cortés-Altamirano et al. (1994) and Cortés-Altamirano and Licea-Durán (1999).
In shrimp ponds from NW Mexico, S. diplococcus was the most abundant species
among cyanobacteria; it was found in all semi-intensive and intensive ponds. On the
contrary, benthic diatoms (Cyclotella spp., Nitzschia spp. and Navicula spp.) represented the least abundant group. Density of diatoms was irregular along the culture
cycle; however, the highest abundance occurred at the last 2 months of the cycle.
Among dinoflagellates, Peridinium trochoideum (Scrippsiella trochoidea) was the
dominant species, while P. minimum and Gymnodinium spp. occurred only occasionally
and in low abundance. From the literature available on microalgal abundance in shrimp
culture ponds for the northwest of Mexico, the most representative genera are included
in Table 6.
6. Harmful algal blooms in shrimp ponds
In semi-intensive shrimp ponds, the relation between phytoplankton quality and
shrimp development has been demonstrated (Dall et al., 1990). However, since
phytoplankton growth is enhanced by the addition of fertilizers, dinoflagellate blooms
also develop. In some cases, dinoflagellate blooms are harmless to shrimp; such is the
case of the formation of Peridinum balechii red tides, which did not result in a loss of
shrimp production (Delgado et al., 1996). In other cases, algal blooms can affect
shrimp development (Mingyuan and Jiansheng, 1993; Cortés-Altamirano and LiceaDurán, 1999). Another negative impact of algal blooms on shrimp production is the
occurrence of brown spots on the specimens; this was the case of shrimp from Ecuador
(Stirling and Day, 1990).
Massive dinoflagellate blooms (red tides) have been documented in shrimp culture
ponds from different regions of the world; such events can turn into an economic loss.
The majority of mentioned species are bloom-forming algae in nutrient-enriched waters
under natural conditions (Table 7). In Taiwan, the toxic (PSP—paralytic shellfish
poisoning) dinoflagellate Alexandrium tamarense (Gonyaulax tamarensis) caused mor-
Table 7
Summary of harmful algal blooms and their effects on shrimp culture ponds
Location
Algae species
Bloom conditions
Max. conc.
(cellsl 1)
Causes
Effects on penaeid
Ref.
P. orientalis
P. orientalis
Bohai Sea, China
Bohai Sea, China
Euglena spp.
Noctiluca scintillans
nutrient-enricheda,b
nutrient-enricheda,b
1.8 106
2 106
Mortality, 100 tons
–
(1)
(1)
P. monodon
–
P. monodon
Bohai Sea, China
Shanghai, China
Taiwan, China
Gymnodinium spp.
Noctiluca scintillans
Alexandrium tamarense
nutrient-enricheda,b
nutrient-enricheda,b
frontal zonea,b
20 106
–
10 106
Mortality, 10,000 tons
Diseases in shrimp
Mortality
(2)
(3)
(4)
–
Do Son, Vietnam
Nitzschia navis-varingica
nutrient-enriched
–
Mortality
(5)
–
Malaysia
Chatonella spp.
nutrient-enricheda,b
–
Camaguey Cuba
Guayaquil, Ecuador
Sinaloa, México
Sinaloa, México
Sinaloa, México
Sinaloa, México
Sinaloa, México
Protoperidinium balechii
Gyrodinium instriatum
Synechocystis diplococcus
Schizothrix calcicola
Prorocentrum minimum
Gymnodinium catenatum
Gymnodinium catenatum
nutrient-enriched
nutrient-enriched
nutrient-enriched
changes in salinity
nutrient enriched
upwellinga,b
upwellinga,b
Mortality, 30 – 45%
loss of harvest
Not detected
Mortality
Growth decrease
Growth decrease
Growth decrease
Nauplii mortality
Nauplii and adult
mortality
(85% pond 1 pumped)
(6)
P. schmittii
L. vannamei
L. vannamei
L. vannamei
L. stylirostris
L. stylirostris
L. vannamei
Anoxia
Anoxia and ammonia
production
Anoxia
–
Poisoning PSP
0.72 10 4 MUc cell
Poisoning ASP
1.7 pg cell 1
Anoxia and mucus
production
–
Anoxia
–
–
–
Poisoning PSPa,b
Poisoning PSPa
0.83 10 4 MUc cell
8000
93.6 106
3.4 106
140 106
34 106
18,000a
15,000a
a
1
1
(7)
(8)
(9)
(10)
(10)
(11)
(12); (13)
—Not reported.
References: (1) Mingyuan and Jiansheng (1993); (2) Jiasheng et al. (1993); (3) Chen and Gu (1993); (4) Huei-Meei et al. (1993): (5) Kotaki et al. (2000); (6) Maclean
(1989); (7) Delgado et al. (1996); (8) Jiménez (1993); (9) Cortés-Altamirano (1994); (10) Cortés-Altamirano and Licea-Durán (1999); (11) Cortés-Altamirano and AlonsoRodrı́guez (1997); (12) Gárate-Lizárraga et al. (2002); (13) this study.
a
Measures or observations in the water source.
b
Natural bloom conditions were obtained from Smayda (2000).
c
MU (1 mouse unit = 0.18 Ag STX).
R. Alonso-Rodrı́guez, F. Páez-Osuna / Aquaculture 219 (2003) 317–336
Cultured
penaeid
327
328
R. Alonso-Rodrı́guez, F. Páez-Osuna / Aquaculture 219 (2003) 317–336
tality of P. monodon in 1989 (Huei-Meei et al., 1993). The same year in China, the
potentially toxic dinoflagellate Gymnodinium spp. produced a $US 40 million loss in
shrimp aquaculture because of oxygen depletion (Jiasheng et al., 1993). Some
flagellates like Euglena spp. can also cause problems when ammonia (metabolic
product) and mucus (abnormal secretion in gills of fishes) are expelled to water and
eventually kill the shrimp Penaeus orientalis or make it vulnerable to diseases
(Mingyuan and Jiansheng, 1993).
Between 1983 and 1985, shrimp production in Malaysia decreased 30– 50% because of
two red tide events produced by a raphidophyte (Hornelia) bloom; this species produces a
silt layer that covers crustacean gills that turn into a brown color (Maclean, 1989). In
Ecuador, the dinoflagellate Gyrodinium instriatum caused shrimp mortality by anoxia in
shrimp farms during 1982 (Jiménez, 1993).
In the natural environment, crustaceans can accumulate toxins in the hepatopancreas
that may affect man through consumption of the whole organism; however, if only muscle
is consumed, toxicity is rarely probable (Shumway, 1995). At times, shrimp toxicity is not
related with algal density, as is the case of small numbers of Pyrodinium bahamense var.
compressum, which produces PSP.
In Brunei Darussalam and Malaysia, P. bahamense var. compressum has been reported
to produce PSP in the natural environment at levels that are below the lowest permitted
level. It has been stated that more than 4 MU g 1 (MU = mouse units) requires the
establishment of a quarantine in order to avoid seafood consumption that might be
contaminated with PSP toxins (Shumway, 1995).
Between 1989 and 1991, several studies in two shrimp (Litopenaeus vannamei)
farms from northern and southern Sinaloa (NW Mexico) (Cortés-Altamirano, 1994)
registered the occurrence of some algae that are considered to be harmful or toxic for
shrimp. The most abundant specimens were cyanobacteria (Anabaena spp., Anabaenopsis elenkinii and O. limnetica); they colonize superficial waters and block light
penetration that results in eutrophic conditions at the bottom of the ponds. In 1989,
there were ponds with high density of O. limnetica and deficient shrimp growth; it was
possibly due to cyanobacteria dominance and scarce density of diatoms (more
nutritious).
Also, some dinoflagellates that are frequently observed are P. minimum, Gymnodinium spp., Gyrodinium spp. and Protoperidinium trochoideum (S. trochoidea). P.
minimum is considered to be a toxic species whose abundance is promoted by humic
acids (Granéli and Moreira, 1990) and an inadequate fertilization (Cortés-Altamirano et
al., 1994). More specific information on the occurrence and taxonomy of P. minimum
in the coastal waters of the Mexican Pacific is presented in diverse studies (CortésAltamirano and Agraz-Hernández, 1994; Cortés-Altamirano et al., 1996; HernándezBecerril et al., 2000).
Between 1990 and 1993, Cortés-Altamirano and Licea-Durán (1999) studied three
shrimp farms from NW Mexico with the aim of detecting algal blooms in shrimp
ponds. They reported that S. diplococcus, a non-toxic cyanobacteria, was frequently
observed. Algal bloom duration ranged from 1 to 10 days; dominant species were
cyanobacteria A. elenkinii, Schizothrix calcicola and Anabaena aequalis, and dinoflagellates P. minimum, Gymnodinium incoloratum, Gyrodinium spirale and other
R. Alonso-Rodrı́guez, F. Páez-Osuna / Aquaculture 219 (2003) 317–336
329
species of the genus Gyrodinium. Several factors were considered to be responsible for
the algal blooms: inadequate fertilization, excretion of substances that promote growth
of microalgae and environmental conditions (including salinity). In a farm, shrimp
weight was lowered because of a S. calcicola bloom associated with strong rains; low
salinity of about 12, an abundance up to 140 106 tricomes l 1 and, in addition, a
diminution in average gained in weight down to 0.1 g week 1 were observed (CortésAltamirano and Licea-Durán, 1999).
During February –May 1997, a massive nauplii mortality in postlarvae laboratories
from southern Sinaloa supposes toxicity coming from supply water and connected
with the occurrence of coastal red tides produced by Ceratium dens, Pseudonitzschia
spp. and Gymnodinium catenatum, but no toxicity in nauplii extract were detected by
the mouse bioassay, which showed poisoning symptoms, with some recovery after an
hour (Cortés-Altamirano and Alonso-Rodrı́guez, 1997). Another event of massive
mortality of nauplii and adults shrimp occurred during February –May 2001 (Fig. 2);
such mortality coincided with a series of G. catenatum red tides in the coast of
Sinaloa. HPLC toxicity analysis on phytoplankton showed the presence of saxitoxin
derivatives as C2 and decarbamoilsaxitoxins, which have relatively low toxicity
(Gárate-Lizárraga et al., 2002). In both cases, the toxicity was low to regulatory
level of 80 Ag STX eq 100 g 1 of edible shellfish (29 and 40 Ag STX eq 100 g 1
Fig. 2. Mass mortality shrimp in ponds in Sinaloa, Mexico after water exchange from coastal waters during red
tides February – May 2001 (this study). Photo donated by Sergio Escutia.
330
R. Alonso-Rodrı́guez, F. Páez-Osuna / Aquaculture 219 (2003) 317–336
oyster tissue, respectively) (Cortés Altamirano and Alonso-Rodrı́guez, 1997; Gárate
Lizárraga et al., 2002).
The diagnosis of harmful phytoplankton species that have been reported in shrimp farm
ponds from NW Mexico are listed below:
(1) A. aequalis Borge filamentous cyanobacteria—forms blooms in brackish waters and
produces unpleasant taste and odor to cultured catfish (Ploeg and Dennis, 1992).
(2) A. elenkinii (Miller 1923) Hungarica Halascz 1939—cyanobacteria that occurs as
simple filaments and forms blooms during the summer when turbidity is high (JeejiBai et al., 1977).
(3) G. incoloratum Conrad and Kufferath 1954—athecate dinoflagellate, a common
inhabitant in estuarine environments that have been affected by human activities
(Mountford, 1984). This species has been associated with diarrhea (Cortés-Altamirano
and Licea-Durán, 1999).
(4) G. spirale (Bergh) Kofoid et Swezy 1921 (Gymnodinium spirale Bergh 1881)—
athecated dinoflagellate, heterotroph, when present in high densities; it has caused
certain toxicity to mollusks in the French coasts (Sournia et al., 1991).
(5) O. limnetica Lemmermann, E. 1907. (Lyngbya limnetica Anagnostidis)—belongs to
cyanobacteria group and can be found in fresh and brackish waters, filamentous, and
has the ability to fix nitrogen when oxygen is present (Caljon, 1983). Generally, the
bloom is during the summer. This species is able to adapt to oxic and sub-oxic
conditions. O. limnetica adapts to changing conditions of the environment and ponds
(Shilo, 1980; Cortés-Altamirano and Licea-Durán, 1999).
(6) P. minimum (Pavillard) Schiller ( P. marie-lebourae (Park and Ballantine, 1957)
Loeblich III 1970; P. triangulatum Martin 1929; Exuviaella minima Pavillard,
1916)—mixotrophic dinoflagellate, with registered strains in Japan, Portugal and
France, produces human poisoning by way of a poison (venerupin) that affects liver;
symptoms are similar to those of poisoning produced by consumption of oysters and
clams. Other strains produce effects that resemble those of PSP (DenardouQueneherve et al., 1999). In shrimp ponds with high densities, this species causes
shrimp stress that affects its growth and makes organisms more vulnerable to viral
diseases like hypodermic and hematopoietic necrosis (Cortés-Altamirano and AgrazHernández, 1994).
(7) S. calcicola (Ag) Gomont—cyanobacteria that is considered as a toxic species,
produces dermatitis; the sea hare (Carpenter and Carmichael, 1995) accumulates this
toxin. The occurrence of this species is related to hemolytic enteritis that possibly
decreases shrimp growth (Cortés-Altamirano and Licea-Durán, 1999).
7. Concluding remarks
1. Physicochemical conditions that originate algal blooms in shrimp ponds mainly
depend on fertilization, feeding rate and food composition. The objective of pond
fertilization is to produce diatom and phytoflagellate blooms; however, inadequate
management, contamination and climatic conditions can trigger undesired blooms
R. Alonso-Rodrı́guez, F. Páez-Osuna / Aquaculture 219 (2003) 317–336
2.
3.
4.
5.
331
that lead to a delay in shrimp growth and massive mortality that decreases
production.
Nutrients that are supplied to shrimp ponds have a direct effect on phytoplankton
production. Depending on the amount of nutrients and their stoichiometric ratio, some
species are more developed. Low rates of N/P enhance nannoplankton dominance in
shrimp ponds, as is the case in coastal and estuarine waters.
A detailed examination of phytoplankton composition in shrimp ponds from NW
Mexico indicates that cyanophyceae are an abundant group; this is different in other
parts of the world where diatoms and dinoflagellates predominate.
In order of abundance, the reported species that form blooms in NW Mexico are the
cyanobacteria S. diplococcus, A. aequalis, A. elenkinii and O. limnetica. According to
their potential toxicity, the species are the dinoflagellates P. minimum, G. incoloratum,
G. spirale, G. catenatum and the cyanobacteria S. calcicola.
From this review, a permanent phytoplankton monitoring by farmers in shrimp ponds
and supply water is necessary to maintain a good quality for the culturing system.
Acknowledgements
CONACyT thought Project 0625-N9110 provided financial support. The first author is
under scholarship from CONACyT 89906. The authors thank Jorge Ruelas Inzunza for
English review of the original manuscript and Sergio Escutia for the information and
image about update shrimp mortality in ponds. We also thank Clara Ramı́rez Jáuregui and
Jahn Throndsen for their collaboration in facilitating the bibliography, and Germán
Ramı́rez Reséndiz for elaborating figures.
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